2.4 Potential Contributions to Understanding Behavioral Mechanisms in Primate Societies
2.4.4 Behavioral Mechanism Promoting Genetic Diversity in a Small Group
Like most nonhuman primates in China, Tibetan macaques live in small, isolated populations. Theoretically, a small population or group may suffer the detrimental effects of inbreeding and the loss of genetic diversity (Spielman et al.2004). Our study group is a medium-sized one with 20–50 individuals and that ranges in a small habitat (Li et al. 1996). However, we have not found conspicuous changes in behavior during the 30-year period, except the sudden death of 17 individuals in the spring of 1988. Although we have noticed a decline in the frequency of affiliative interactions among group members and an increase in infant mortality in recent years, these appear to be a side effect of provisioning, which increases the rate of aggression among group members (Berman and Li2002).
Additionally, we found that our study group has a relatively high haplotype diversity (Hd ¼ 0.341) when compared to other subspecies (M. t. pullus, Hd¼ 0.222; M. t. guizhouensis, Hd ¼ 0.478) (Sun et al.2010). As such, loss of genetic diversity may not be a major concern in our study group at present. It is likely that some behavioral mechanisms in this group may play an important role in preventing or slowing down the loss of genetic diversity that is often observed in small groups. For instance, we found that the transfer of males into and out of the group occurs annually (Li et al.1996). Also, kin recognition may prevent mating between matrilineal relatives. In fact, one of our studies demonstrates that no copulation involved mother-son dyads, and only 2.1% (7/329) of copulations were
success. The medium-sized group of Tibetan macaques we study facilitates censuses and unambiguous identification of all group members in the field. As the largest macaque species with a relatively male-biased adult sex ratio and year-round mating but seasonal birth, this species offers a large spectrum of sociodemographic condi-tions conducive for testing hypotheses related to dominance style and groupfission.
Furthermore, a rich repertoire of affiliative and ritualized behaviors and a complex interplay of competitive and cooperative relationships, especially among males, can provide primatologists with a wealth of opportunities to pursue additional behav-ioral, ecological, and evolutionary research projects focused on Tibetan macaques.
Acknowledgments Our long-termfield study has been supported by Anhui University and the Huangshan Garden Bureau. Our research would be impossible without their assistance in terms of permission, personnel, funding, and other logistic support. For more than three decades, many researchers and students, especially those from Anhui University, Kyoto University, State Univer-sity of New York at Buffalo, UniverUniver-sity of Washington, and Central Washington UniverUniver-sity, have joined and contributed to the study. We cordially thank Qi-Shan Wang, Kazuo Wada, Cheng-Pei Xiong, Guo-Qiang Quan, He-Ling Shen, Ren-Mei Ren, Ming Li, Jiao Shao, Zu-Wang Wang, Zhi-Gang Jiang, Kunio Watanabe, Hideshi Ogawa, Frans de Wall, Noel Rowe, Carol Berman, Consuel Ionica, Lei Zhang, Toshisada Nishida, Randall Kyes, Lisa Jones-Engel, Lixing Sun, Lori Sheeran, Megan Matheson, Steven Wagner, Dong-Po Xia, Bing-Hua Sun, Yong Zhu, Xi Wang, Yang Liu, Jian-Yuan Zhao, Jessica Mayhew, and Paul Garber for their full-hearted supports and noted contributions. We also express our thanks to Fu-Wen Wei, Bao-Guo Li, Yan-Jie Su, Cheng-Ming Huang, Xue-Long Jiang, Ji-Qi Lu, and other members of China Primatology Society. This work wasfinancially supported by the National Natural Science Foundation of China, the China Scholarship Council, the Key Teacher Program of the Ministry of Education of China, the Outstanding Youth Foundation of Anhui Province, the International Science and Technology Cooperation Plan of Anhui Province, Natural Science Foundation of Anhui Province, Inoue Scientific fund, Primate Conservation Inc., the L.S.B. Leakey Foundation, the Wenner-Gren Foundation, the ASP Conservation Small Grant, and the National Natural Science Foundation.
Special thanks to Mr. Cheng’s family and Fuxi villagers for their outstanding logistic support during ourfield observation for more than three decades.
Pedigree of the YA1 social group of Tibetan macaques in Huangshan (September, 2017). Note: The pedigree was mapped based on maternal relationships of three matrilines. Males with known identities were also included. Letters under the blue squares (males) or red circles (females) represent individual names. Question marks indicate the identity of males are yet to be unknown
3 Chase An individual stares at the recipient and rushes at him/her at great speed. The recipient typicallyflees.
4 Seize The performer grabs the body, face, neck, or ear of the recipient with one hand, shakes it, and then releases it. Sometimes the performer also comes very close (face to face) and stares at the recipient.
Picture3
5 Bite The performer grabs the receiver tightly, preventing him/her
fromfleeing, and bites the recipient vigorously. Picture4 6 Avoid The performer turns its body away from the attacker as if
preparing toflee while displaying a “horrified” facial expression toward the attacker.
Picture5
7 Flee The target of an attack will run in the opposite direction from the attacker.
8 Scream A vocal reaction to an attacker. The scream is high pitched and of long duration. This may be accompanied byfleeing.
Picture6
9 Redirection When A is attacked by B, A responds immediately by attacking C. C is an individual that is nearby and lower-ranking than both A and B. In some cases, B will join the attack against C.
Picture7
10 Solicit support When an individual is attacked by another individ-ual, it intermittently scans the attacker and a higher-ranking individual nearby with screams. The higher-ranking bystander may respond by interrupting the attack on the scanner.
Picture8
11 Hold bottom The performer (usually the alpha female) approaches one of two other females that are engaged in afight. She approaches from behind and holds the bottom of the female.
Both females typically teeth-chatter to one another. This tends to interrupt thefight.
Picture9
12 Approach An individual moves directly toward another individual, coming within 1 m.
13 Leave An individual moves from within 1 m to more than 1 m of another individual.
Picture10
14 Proximity Two or more individuals are sitting or lying within 1 m or between 1 and 5 m (depending on studies).
Picture11
(continued)
involving two or more individuals include chase, mock fight, and combinations of previous behavior.
18 Social grooming/
allogrooming
One individual uses his/herfingers and palms to groom the fur of another individual. The groomer may pick out small objects from the recipients fur and eat them.
Picture15
19 Embrace Two individuals, usually adult males, hold each other while face to face. Each partner will reach with one hand and attempt to touch the genitals of the other. Both partners typically teeth-chatter and vocalize excitedly.
Picture16
20 Touch A ritualistic behavior between males in which the lower-ranking individual approaches the higher-lower-ranking individual in front. The higher-ranking male touches some part of the body of the lower-ranking individual (head, back, shoulder).
Then the lower-ranking individual leaves. This may be used in a tense situation and appears to be a means by which the lower-ranking individual obtains“permission” to proceed on its pathway or with its apparent goal.
21 Present One individual approaches the front of the other and shows his bottom to the other. Usually the presenter is the lower-ranking of the two partners. Females also present to males.
Picture17
22 Mount One male (usually the lower-ranking) grabs the back hair of another male and mounts from behind, using the full ankle clasp posture. Both males teeth-chatter and scream excit-edly. Then the mounter dismounts. The duration of the mount is about 3–5 s. This may be a simple friendly gesture or a post-conflict behavior.
Picture18
23 Show penis This is a ritualized behavior shown by juvenile males toward adult males. Usually, the lower-ranking male approaches the higher-ranking male, raises one leg, and displays his penis.
The higher-ranking male puts his head on the belly of the lower-ranking male and licks or touches the penis with his hand. The juvenile may show his penis from a reclining position.
Picture19
24 Suck penis A young male approaches an adult male and jumps on his head. The adult male holds the younger male by the waist in such a way that his mouth can reach the young male’s penis.
The adult sucks the young male’s penis and then the youn-ger male leaves.
Picture20
(continued)
triad with excitement as if they wish to participate.
27 Genital inspection
One individual will touch the genitals—the vagina of a female or the anus of a male—and sniff it or lick it directly.
When a male inspects a female in estrus, it is called a sexual inspection.
Picture23
28 Sexual inspection
A genital inspection by an adult male of an estrus female. Picture24
29 Sexual chase An adult male chases a female and attempts to mate with her. The sexual chase differs from the aggressive chase in that it is slower and is interrupted by pauses. In addition, although the female attempts to avoid the male, she is less likely to scream.
Picture25
30 Sexual grimace
An individual directs a grimace toward an adult of the opposite sex that may be either nearby or far away. The male sways his body in a manner that makes him more noticeable to the female. The grimace differs from a fear grimace in that the corners of the mouth are not drawn back as far. This is a sexual solicitation.
Picture26
31 Mating Three types of mating are described: (1) intromission and thrusting only; (2) intromission, thrusting, and pausing; and (3) intromission, thrusting, pausing, and calling.
Picture27
32 Harassment Individuals approach a mating pair excitedly, touch the heads, lick, or stick their faces in the faces of the mating partners. They may also grimace or scream. This does not generally interrupt the copulation of the mating partners.
Picture28
33 Consortship An adult male and female form a temporary close affiliative and sexual relationship during the mating season. They will move, feed, mate, and groom together, but do not neces-sarily mate exclusively with one another. Their frequencies of following one another are much higher than during non-mating periods.
Picture29
Picture 1 An individual stares another animal
Picture 2 The right adult male slaps toward his front individual
Picture 3 An adult male (middle) seizes another adult male (right)
Picture 4 An adult male bites another adult male (two monkeys in right)
Picture 5 An adult male (right) avoids adult male’s (middle) aggression
Picture 6 An adult female (right) screams when she is attacked by adult male (left)
Picture 7 The middle adult male redirects aggression from right adult male to the left adult male
Picture 8 The middle adult male is getting the left male’s support when he is in conflict with the right adult male
Picture 9 An adult male holds the button of a juvenile male (left)
Picture 10 The right adult male is leaving left adult male
Picture 11 An adult male (left) is in proximity with an adult female within 1 m
Picture 12 An adult female (left) is following an adult male
Picture 13 Teeth chatting
Picture 14 Three juveniles play together
Picture 15 Social grooming between two females
Picture 16 Embrace
Picture 17 An adult male presents to another male
Picture 18 Male–male mount
Picture 19 Show the penis
Picture 20 A juvenile (left) is sucking an infant’s penis
Picture 21 An adult male holds an infant
Picture 22 Male–male bridging
Picture 23 Genital inspection
Picture 24 Sexual inspection
Picture 25 An adult male (left) chases an adult female (right) for mating
Picture 26 An adult male (right) grimace to an adult female (left)
Picture 27 An adult male (left) is mating with an adult female (right)
References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–266 Berman C, Li JH (2002) Impact of translocation, provisioning and range restriction on a group of
Macaca thibetana. Int J Primatol 23:283–397
Berman C, Ionica C, Li JH (2004) Dominance style among Macaca thibetana on Mt. Huangshan, China. Int J Primatol 25:1283–1312
Berman C, Ionica C, Dorner M, Li JH (2006) Postconflict affiliation between former opponents in Macaca thibetana on Mt. Huangshan, China. Int J Primatol 27:827–854
Deag J, Crook J (1971) Social behaviour and“agonistic buffering” in the wild Barbary macaque Macaca sylvana L. Folia Primatol 15:183–200
Delson E (1980) Fossil macaques, phyletic relationships and a scenario of development. In:
Lindburg D (ed) The macaques: studies in ecology, behavior, and evolution. Van Nostrand Reinhold, New York, pp 31–51
Picture 28 An adult male (left) is harassing a mating pair
Picture 29 An adult male (right) forms consortship with an adult female (left)
Li JH, Wang QS (1996) Dominance hierarchy and its chronic change in adult male Tibetan macaques (Macaca thibetana). Acta Zool Sin 42:330–334
Li JH, Wang QS, Li M (1994) Studies on population ecology of Tibetan monkeys (Macaca thibetana). II. Reproductive pattern of Tibetan monkeys. Acta Therlol Sin 14(4):255–259 Li JH, Wang QS, Han DM (1996) Fission in a free-ranging Tibetan macaque group at Huangshan
Mountain, China. Chin Sci Bull 41:1377–1381
Li JH, Yin HB, Wang QS (2005) Seasonality of reproduction and sexual activity in female Tibetan macaques (Macaca thibetana) at Huangshan, China. Acta Zool Sin 51:365–375
Li JH, Yin HB, Zhou LZ (2007) Non-reproductive copulation behavior among Tibetan macaques (Macaca thibetana) at Huangshan, China. Primates 48:64–72
Li DM, Fan LG, Ran JH, Yin HL, Wang HX, Wu SB, Yue BS (2008) Genetic diversity analysis of Macaca thibetana based on mitochondrial DNA control region sequences. DNA Seq 19 (5):446–452
Liu Y, Li JH, Zhao JY (2006) Sequence variation of mitochondrial DNA control region and population genetic diversity of Tibetan macaques Macaca thibetana in the Huangshan Moun-tain. Acta Zool Sin 52(4):724–730
Macintosh A, Huffman M, Nishiwaki K, Miyabe-Nishiwaki T (2012) Urological screening of a wild group of Japanese macaques (Macaca fuscata yakui): investigating trends in nutrition and health. Int J Primatol 33(2):460–478
Matheson M, Sheeran L, Li JH, Wagner R (2006) Tourist impact on Tibetan macaques. Anthrozoös 19:158–168
Matsumura S (1999) The evolution of “egalitarian” and “despotic” social systems among macaques. Primates 40:23–31
Ogawa H (1995a) Bridging behavior and other affiliative interactions among male Tibetan macaques (Macaca thibetana). Int J Primatol 16:707–729
Ogawa H (1995b) Recognition of social relationships in bridging behavior among Tibetan macaques (Macaca thibetana). Am J Primatol 35:305–310
Ogawa H (2019) Bridging behavior and male-infant interactions in Macaca thibetana and M. assamensis: insight into the evolution of social behavior in the sinica species-group of macaques. In: Li J-H, Sun L, Kappeler P (eds) The behavioral ecology of the Tibetan Macaque.
Springer, Heidelberg
Pan RL, Jablonski N, Oxnard C, Freedman L (1998) Morphometric analysis of Macaca arctoides and M. thibetana in relation to Other Macaque species. Primates 39(4):519–537
Simons N, Lorenz J, Sheeran L, Li JH, Xia DP, Wagner R (2012) Noninvasive saliva collection for DNA analysis from free-ranging Tibetan macaques (Macaca thibetana). Am J Primatol 74:1064–1070
Smuts BB (1985) Sex and friendship in baboons. Aldine, Hawthorne, NY
Smuts B, Cheney D, Seyfarth R, Wrangham R, Struhsaker T (1987) Primate society. University of Chicago Press, Chicago, IL
Spielman D, Brook B, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci U S A 101:15261–15264
Stanford C (1992) The costs and benefits of allomothering in wild capped langurs (Presbytis pileata). Behav Ecol Sociobiol 30:29–34
Chin J Wildlife 29:6–10
Waters S, Harrad A, Chetuan M, Amhaouch Z (2015) Barbary macaque group size and composition in Bouhachem forest, north Morocco. Afr Primates 10:53–56
Xia DP, Li JH, Garber P, Matheson M, Sun BH, Zhu Y (2013) Grooming reciprocity in male Tibetan macaques. Am J Primatol 75:1009–1020
Xiong CP (1984) Studies on the ecology of Tibetan monkeys. Acta Theriol Sin 4:1–9
Xiong CP, Wang QS (1988) Seasonal habitat used by Tibetan monkeys. Acta Theriol Sin 8:176–183
Xiong CP, Wang QS (1991) A comparative study on the male sexual behavior in Thibetan and Japanese monkeys. Acta Theriol Sin 11:13–22
Zhang M, Li JH, Zhu Y, Wang X, Wang S (2010) Male mate choice in Tibetan macaques Macaca thibetana at Mt. Huangshan, China. Curr Zool 56:213–221
Zhang D, Xia DP, Wang X, Zhang QX, Sun BH, Li JH (2018) Bridging may help young female Tibetan macaques Macaca thibetana learn to be a mother. Sci Rep 8:16102
Zhao QK (1993) Sexual behavior of Tibetan macaques at Mt. Emei, China. Primates 34(4):431–444 Zhao QK (1996) Male-infant-male interactions in Tibetan macaques. Primates 37(2):135–143 Zhao JY, Li JH, Liu Y, Yin HB (2005) Research on DNA extraction from old feces of Macaca
thibetana. Acta Theriol Sin 25:410–413
Zhu Y, Li JH, Xia DP, Chen R, Sun BH (2008) Inbreeding avoidance by female Tibetan macaques Macaca thibetana at Huangshan, China. Acta Zool Sin 54:183–190
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